Behavioural Processes 130 (2016) 4–10
Contents lists available at ScienceDirect
Behavioural Processes
journal homepage: www.elsevier.com/locate/behavproc
Multimodal communication, mismatched messages and the effects of
turbidity on the antipredator behavior of the Barton Springs
salamander, Eurycea sosorum
Kristina C. Zabierek, Caitlin R. Gabor ∗
Department of Biology, Population and Conservation Biology Program, Texas State University, San Marcos, TX, USA
a r t i c l e
i n f o
Article history:
Received 11 March 2016
Received in revised form 22 May 2016
Accepted 27 June 2016
Available online 28 June 2016
Keywords:
Amphibian
Chemical cue
Darter
Sensory compensation
Sunfish
Visual cue
a b s t r a c t
Prey may use multiple sensory channels to detect predators, whose cues may differ in altered sensory
environments, such as turbid conditions. Depending on the environment, prey may use cues in an additive/complementary manner or in a compensatory manner. First, to determine whether the purely aquatic
Barton Springs salamander, Eurycea sosorum, show an antipredator response to visual cues, we examined
their activity when exposed to either visual cues of a predatory fish (Lepomis cyanellus) or a non-predatory
fish (Etheostoma lepidum). Salamanders decreased activity in response to predator visual cues only. Then,
we examined the antipredator response of these salamanders to all matched and mismatched combinations of chemical and visual cues of the same predatory and non-predatory fish in clear and low
turbidity conditions. Salamanders decreased activity in response to predator chemical cues matched
with predator visual cues or mismatched with non-predator visual cues. Salamanders also increased
latency to first move to predator chemical cues mismatched with non-predator visual cues. Salamanders
decreased activity and increased latency to first move more in clear as opposed to turbid conditions in all
treatment combinations. Our results indicate that salamanders under all conditions and treatments preferentially rely on chemical cues to determine antipredator behavior, although visual cues are potentially
utilized in conjunction for latency to first move. Our results also have potential conservation implications, as decreased antipredator behavior was seen in turbid conditions. These results reveal complexity
of antipredator behavior in response to multiple cues under different environmental conditions, which
is especially important when considering endangered species.
© 2016 Published by Elsevier B.V.
1. Introduction
The use of multiple sensory channels by prey can improve localization, resolution, and amplification of predator cues (Johnstone,
1996). Aquatic prey may use a combination of cues such as visual,
chemical, tactile, and electric cues in predator detection (Collin
and Whitehead, 2004; Park et al., 2008; Ward and Mehner, 2010;
Hettyey et al., 2012). Prey should use the cue (or multiple cues) that
provides the most certainty of predator threat (Lima and Steury,
2005), which may change based on cue availability and the physical sensory environment (Endler, 1993). Further, use of multimodal
cues can be integrated in an additive manner, triggering a greater
response than use of unimodal cues, consistent with the sensory
∗ Corresponding author at: Department of Biology, Population and Conservation Biology Program, Texas State University, 601 University Drive, San Marcos, TX,
78666, USA.
E-mail address: [email protected] (C.R. Gabor).
http://dx.doi.org/10.1016/j.beproc.2016.06.016
0376-6357/© 2016 Published by Elsevier B.V.
complement hypothesis (Lima and Steury, 2005). Alternatively,
prey may rely primarily on one sensory cue based on their perception or respond in a compensatory manner depending on how the
physical environment influences perception of the cues (i.e., turbid vs clear water: Hartman and Abrahams, 2000; Weissburg et al.,
2014). Some organisms rely on visual cues for predator detection
due to the high information content of visual cues (Hemmi, 2005).
However, in some studies with amphibians, chemical cues have
been found to affect behavior more than visual cues (Stauffer and
Semlitsch, 1993; Kiesecker et al., 1996; Hickman et al., 2004). Testing animals in different environments with a combination of cues
can determine which hypothesis for cue use is supported for a given
species.
The use of sensory modalities by prey has frequently been found
to be dependent on the way the sensory environment affects each
cue (Endler, 1993; Weissburg et al., 2014). Turbidity is a form of
environmental noise that decreases penetrability of light within
the water column and can affect the visual and chemical envi-
K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
ronment for prey (Utne-Palm, 2002). In habitats where turbidity
reduces visual information, some fish compensate for the reduced
visual information by increasing antipredator response to chemical cues (Hartman and Abrahams, 2000; Leahy et al., 2011; Ranåker
et al., 2012). Further, turbidity can yield a mismatch between visual
and chemical cues because turbidity can differentially attenuate
certain wavelengths (Walmsley et al., 1980). This indicates that in
turbid conditions there may be issues with reliance on multimodal
cues for increasing resolution of predator detection because the
cues are more likely to become mismatched. Ward and Mehner
(2010) found that mosquitofish, Gambusia holbrooki, with access
to mismatched cues were faster to approach predator visual cues
than those with matched visual and chemical cues. These findings may be due to non-adaptive antipredator behavior in turbid
conditions or due to predator inspection as an adaptive response
to uncertainty. Either way, response to mismatched cues is predicted to differ from matched cues if there is an additive response,
especially in clear conditions whereas if an organism uses cues
compensatorally then they will only respond to the cue they perceive more strongly in a given environment and use a different cue
if their primary cue is harder to perceive. Therefore, the effect of
turbidity on antipredator behavior likely depends on the mode of
cue use by prey.
Anthropogenic activity such as land development, severe
storms, and recreation have increased turbid conditions in waterways, making turbidity an increasing issue for aquatic organisms
(Henley et al., 2000; Davies-Colley and Smith, 2001). Much of the
work examining behavioral and life history impacts of turbidity has been on fish (Abrahams and Kattenfeld, 1997; Gadomski
and Parsley, 2005; Ferrari et al., 2010a; Swanbrow Becker and
Gabor, 2012; Chivers et al., 2013), but amphibians also suffer
from increased turbidity (Secondi et al., 2007; Schmutzer et al.,
2008). Turbidity can reduce antipredator behavior in aquatic prey
(Gregory, 1993; Miner and Stein, 1993), can decrease generalized predator recognition (Ferrari and Chivers, 2009; Chivers et al.,
2013), and can increase mortality (Horppila et al., 2004).
The Barton Springs salamander, Eurycea sosorum, is a federally
endangered, IUCN red list species (IUCN, 2013) that is neotenic,
fully aquatic, and endemic to Barton Springs, Austin, Travis County,
Texas. In these spring habitats, fish predators abound including redbreast sunfish, Lepomis auritus, and largemouth bass, Micropterus
salmoides (Labay et al., 2011). Further, E. sosorum is threatened
by water quality degradation due to increased recreational use,
increased land development, and reduced spring flow (Dries et al.,
2013), which can increase turbidity (Feng et al., 2012). The turbidity
levels of Barton Springs are typically <1 Nephelometric Turbidity
Units (NTU), but can spike to ∼40 NTU after rain events (White
et al., 2003). NTU’s measure how much light is reflected off of
suspended solids, with higher reflectance (higher NTU’s) corresponding to more suspended solids in a water column. Eurycea
sosorum is often found in clear conditions and avoids silty turbid
habitat (Dries et al., 2013). Therefore, increased turbidity might
affect the ability of E. sosorum to detect and respond to predators if
they are unable to compensate for loss of sensory information, or if
the sensory information becomes mismatched, potentially decreasing their likelihood of survival in a predatory situation.
Eurycea sosorum (captive-reared) show innate antipredator
response to the chemical cues of redbreast sunfish in clear water
(Desantis et al., 2013). However, no study has determined whether
E. sosorum use visual cues for antipredator response or whether
turbidity has a significant effect on antipredator behavior, though
Thaker et al. (2006) found that closely related E. nana show association preferences based on chemical cue or visual and chemical, but
not visual alone. We tested whether individuals of E. sosorum use
visual cues for predator recognition by examining activity of E. sosorum in response to visual cues of two sympatric species: predatory
5
green sunfish, L. cyanellus and non-predatory greenthroat darter,
Etheostoma lepidum.
We also explored cue use of salamanders in response to predators and whether salamanders alter their behavior in response to
turbidity. We exposed salamanders to visual and chemical cues of
predatory and non-predatory fish, either matched or mismatched
in all possible combinations, in both clear and turbid conditions. We
wanted to determine a) whether salamanders use visual cues, b)
the response of salamanders to mismatched vs. matched cues, and
c) the effect of turbidity on response to mismatched vs. matched
cues. Our experimental method will also help discern the mechanism/pattern of multimodal cue use in salamanders and whether
their behavior supports the additive or compensatory hypotheses
for cue use. If salamanders use cues in a complementary/additive
manner, then in clear environments we predict them to show
stronger antipredator response to matched visual and chemical
cues of predators but less to mismatched cues. In turbid conditions
we expect decreased antipredator response compared to matched
cues in clear conditions. If organisms use sensory compensation,
then in turbid environments where visual cues are diminished,
we predict that they will compensate for loss of vision by using
chemical cues.
2. Experiment 1
2.1. Animal maintenance (for both experiments)
We conducted trials at the San Marcos Aquatic Resources Center
(SMARC) in San Marcos, Texas, from June–August 2014 and 24–27
April 2015 between 0800–1800 h. We housed salamanders in large
flow-through fiberglass tanks (61 cm D × 81 cm W × 180 cm L) with
recirculating, temperature-controlled (21–23 ◦ C) well water. We
collected three similarly sized adult green sunfish (L. cyanellus,
mean standard length ± SE = 157 ± 5.84 mm) via hand-line on site
at the SMARC, which we housed in a large flow-through tank partitioned into three equal sections. Davis et al. (2012) found that E.
nana (a close relative to E. sosorum) show antipredator response
to the chemical cues of green sunfish. We collected fourteen similarly sized adult greenthroat darters (E. lepidum: mean standard
length ± SE = 49 ± 0.84 mm) via dip-net from Comal Springs, Texas,
which we housed in three 9.5 l flow-through tanks. Davis & Epp
(unpublished data) found that Eurycea nana (captive-bred) did not
show antipredator response to chemical cues of the closely related
fountain darters, Etheostoma fonticola, and that using darter chemical cue was an equivalent control to water. We maintained all
animals on a 12:12 h light/dark cycle and we fed them live blackworms (Lumbriculus variegatus) and copepod/amphipod mixtures
ad libitum.
2.2. Methods: visual cues
We tested 39 captive-bred, predator naïve, second-generation,
adult E. sosorum in response to the visual cues of (1) four nonpredatory adult greenthroat darters, and (2) one predatory adult
green sunfish. Our set-up consisted of two adjacent 9.5 l drip-flow
tanks filled with 4.5 l of well water with an opaque divider between
the tanks. We placed the salamander in one tank and the fish in the
other. Neither species of fish moved much while in the test tanks
so we did not quantify their movements. To quantify antipredator behavior in each trial we first allowed each salamander to
acclimate for ≥20 min. Following acclimation, we recorded prestimulus activity levels as the amount of time in ambulatory activity
(i.e., swimming or walking) for 8 min (Following Epp and Gabor,
2008). We recorded activity because decreased activity is associated with decreased risk of predation in many aquatic organisms
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K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
3. Experiment 2
3.1. Methods: matched and mismatched visual and chemical cues
Fig. 1. Mean pre and post activity (s) ± SE of Eurycea sosorum to visual cues of a
predatory (sunfish) and non-predatory (darter) fish in clear water. The light color
indicates the pre-stimulus activity and the dark color indicates the post-stimulus
activity. Asterisks represents significant differences of p < 0.05.
when exposed to sit-and-wait predators (Skelly, 1994; Kats and
Dill, 1998; Epp and Gabor, 2008). We then introduced visual cues
by removing the opaque divider and exposing the visual stimulus of
either one adult green sunfish or four adult greenthroat darters (to
provide similar size stimulus to a sunfish) in a clear tank adjacent to
the focal salamander. In order to be consistent with the design for
experiment 2, we also injected 50 ml of clean well water (a control
to simulate cue introduction) with a 60-ml syringe attached to airline tubing 10 cm below the surface of the water at a rate of 2 ml/sec
(following Epp and Gabor, 2008). We then flushed the tubing with
an additional 50 ml of well water at the same rate.
After removing the divider and introducing the water control,
we recorded the amount of time E. sosorum spent active for another
8 min to determine post-stimulus antipredator behavior. Following the experiment, individuals were sexed (Gillette and Peterson,
2001) and had their snout-vent length (SVL) measured before
being placed into a separate tank for tested individuals. We used
3% hydrogen peroxide and water to clean tanks of chemical cues
between trials (Epp and Gabor, 2008).
We tested 200 captive-bred, predator naïve, second-generation,
adult E. sosorum (SVL > 19 mm; Tupa and Davis, 1976) in response
to a native predator, green sunfish, and a non-predator control,
greenthroat darter. We tested two visual cue treatments and two
chemical cue treatments across two vision levels (2 × 2 × 2 design):
(1) clear (0 NTU), and (2) turbid (mean ± SE: 20 ± 0.4 NTU). We
tested the following combination of cue treatments: (1) matched
non-predator visual cues paired with non-predator chemical cues
(darter control cues; n = 25 × 2) (2) mismatched non-predator
visual cues with predator chemical cues (n = 25 × 2), (3) matched
predator visual cues with predator chemical cues (n = 25 × 2), (4)
mismatched predator visual cues with non-predator chemical cues
(n = 25 × 2: Fig. 2). We did not use salamanders more than once for
any treatment and we randomly assigned them to their cue treatments using a random number generator. Prior studies from our
laboratory have shown that the pre- and post-stimulus activity do
not differ when well water cues are introduced in this species and
their close relatives, E. nana (Epp and Gabor, 2008; Desantis et al.,
2013), therefore the pre-treatment activity functions as a control.
This experiment followed the same basic protocol as experiment 1, with the addition of latency as a response variable and
turbidity as a treatment. Following introduction of the chemical
and visual cues, we measured time spent active and additionally
we recorded latency to first move. Latency to first move is defined
as the number of seconds before ambulatory activity was observed.
It is also an important measure of antipredator behavior because
the longer it takes for cryptic prey to resume activity, the more
likely they are to avoid predation, to an extent (Brown and Cowan,
2000; Martín et al., 2009). For turbidity treatments, we added about
2.5 g of bentonite (Sturgis Rock Solid Solutions) to well water and
stirred vigorously while using an aerator to maintain suspension,
prior to salamander acclimation. An aerator was placed in all treatment tanks to maintain consistency throughout the trials. Turbidity
levels were measured at the end of each trial using a calibrated
turbidity meter (Hach 2100N Turbidimeter).
3.2. Chemical cue acquisition
We performed a paired t-test to determine whether prestimulus vs post-stimulus activity differed for each treatment (a
significant difference in the predator treatment indicates that the
pre-stimulus trial also suffices as a control).
Chemical cues were collected by placing each fish in a volume
of water proportional to their displacement (230 ml water per 1 ml
displacement) for 24 h, after which cues were pooled across individuals of the same species, and frozen until day of use (Mathis
et al., 2003; Epp and Gabor, 2008). The same individual recorded
all behavior (KZ) and was blind to chemical cue treatment by coding
chemical cues.
2.4. Results
3.3. Data analysis
Salamanders decreased activity in the presence of the visual
cues of predatory sunfish (t = −2.68, df = 18, p = 0.02). Salamanders
did not change their activity in the presence of the visual cues of a
non-predatory darter (t = 0.12, df = 18, p = 0.91; Fig. 1).
We conducted a repeated measures ANOVA on pre vs. post activity as response variables and cue treatment (four combinations) and
turbidity as independent variables, followed by a matched pairs
post hoc test. In order to determine whether there was a difference
in activity due to turbidity alone, irrespective of treatment, we performed a t-test of all pre-treatment salamanders, using time active
as the response variable and turbidity as the independent variable.
We conducted a two-way ANOVA using latency to first move as a
response variable and cue treatment (four combinations) and turbidity as independent variables followed by a post-hoc Tukey’s HSD
test and a power analysis. We tested data normality and equality
of variances using a Shapiro-Wilk and Levene’s tests, respectively.
We used a square root transformation to improve data normality.
2.3. Data analysis
2.5. Discussion
We found that E. sosorum can use visual cues for predator
recognition; in the absence of chemical cues, salamanders showed
antipredator behavior (decreased activity) in response to visual
cues of a predator, but did not respond to visual cues of four nonpredatory darters. The response to the predatory fish is consistent
with predator recognition.
K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
7
Fig. 2. Schematic of fully-crossed experimental design involving chemical cues and visual cues of predator (Lepomis cyanellus) vs. non-predator (Etheostoma lepidum), in
clear (0 NTU) and turbid (∼20 NTU) conditions.
We removed two values that were outliers based on Shapiro-Wilk
test. All analyses were performed in JMP Pro (11.2.1).
matched or matched with non-predator or predator visual cues.
Salamander behavior did not change in response to any combinations containing non-predator chemical cues.
3.4. Results
4. Discussion
There was a significant effect of turbidity on pre and post activity, with salamanders decreasing activity more in clear vs turbid
conditions (F1,186 = 5.32, p = 0.02; Fig. 3a). There was no significant
difference in pre-treatment activity among salamanders in clear
and turbid conditions (t (192) = 0.706, p = 0.48, 95% CI [-10.2, 21.6]).
There was also a significant interaction between activity (time)
and treatment (F3,186 = 4.53, p = 0.004) and turbidity (F1,186 = 4.93,
p = 0.03; Fig. 3b). We found that salamanders decreased activity in response to predator chemical cue matched with predator
visual cues (t = −4.13, df = 46, p = 0.0002) or mismatched with
non-predator visual cues (t = −5.03, df = 47, p < 0.0001). No other
treatments were significant.
There was a significant effect of treatment (F3,166 = 4.14,
p = 0.007) and turbidity (F1,166 = 7.16, p = 0.008; Fig. 3c) on latency
to first move. There were no significant interactions between treatment and turbidity. Salamanders increased latency to first move
more in response to predator chemical cues mismatched with
non-predator visual cues than to non-predator chemical cue either
matched or mismatched with visual cue (p < 0.05; Fig. 3c). Latency
to first move did not differ for mixed and matched cues when the
chemical cue was from the predator (p > 0.05; ß = 0.84; Fig. 3c).
Latency to first move did not differ for matched predator cues with
mixed or matched cues when the chemical cue was from the nonpredator (p > 0.05; Fig. 3c). Salamanders increased their latency to
first move more in clear (mean ± SE: 8.75 ± 0.57) as opposed to
turbid conditions (mean ± SE: 6.68 ± 0.53).
3.5. Discussion
Salamanders decreased their activity and increased their latency
to first move more in clear conditions than in turbid conditions.
Salamander pre-stimulus activity did not differ between turbid and
clear conditions, indicating that the change in behavior was driven
by the treatment. Salamanders also showed greater antipredator
response (freezing) to chemical cues of predators when mis-
We examined antipredator response of an aquatic salamander to
multiple cues under different environmental conditions. We tested
salamander response to mismatched and matched cues in clear
and low turbidity conditions. Our results suggest that salamanders
use chemical cues over visual cues preferentially, despite having
the ability to use visual cues, and that they decrease activity and
increase latency to respond more in clear conditions than turbid
conditions.
Our findings do not support the additive or compensatory
patterns for cue use in antipredator behavior. Contrary to the
prediction that the interaction between sensory modalities is
dependent on how the sensory environment affects each cue, we
found no interaction between turbidity and cue treatment. This
suggests that salamanders are not changing their response to different cues depending on the environmental conditions. Instead,
salamanders only decreased total antipredator response (i.e., less
decrease in activity and decreased latency to first move) in turbid
water, not in clear conditions. Our results indicate that low turbidity levels are associated with a decrease in antipredator behavior
of this aquatic species found in clear springs, which may contribute
to population declines.
Salamanders did not decrease activity to matched non-predator
chemical and visual cues, indicating that these salamanders do
not perceive darters as predators, as previously found by Davis
& Epp (unpublished data). Further, salamanders did not show
antipredator behavior towards mismatched non-predator chemical cues with predator visual cues, but responded to mismatched
and matched visual cues with chemical cues of predators. Given
the results of the first experiment, this lends support that salamanders preferentially use chemical cues of predators over visual cues
when both are present, instead of compensating or complimenting chemical cues with visual cues. Similarly, amphibian prey have
been found to discriminate between predators and non-predators
in response to chemical cues, but exhibited antipredator behavior
8
K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
Fig. 3. (A) Mean pre and post activity (s) ± SE of Eurycea sosorum in clear vs turbid water. Salamanders decreased activity more in clear water than turbid water. The light color
indicates the pre-stimulus activity and the dark color indicates the post-stimulus activity. Asterisks represents significant differences of p < 0.05. (B) Mean activity pre and
post (s) ± SE of Eurycea sosorum in response to both predator (sunfish) and non-predator (darter) visual and chemical cues. Salamanders decreased activity more in response
to the predatory chemical cues, both mismatched and matched with visual cues of predators and non-predators, compared to all other treatments. The light color indicates
the pre-stimulus activity and the dark color indicates the post-stimulus activity. Asterisks represents significant differences of p < 0.05. (C) Mean latency (untransformed) to
first show ambulatory activity (s) ± SE of Eurycea sosorum after introduction of chemical and visual cues of predatory sunfish and non-predatory darters in clear and turbid
water. Salamanders increased latency to move in response to mismatched predator chemical cues, compared to both matched and mismatched non-predator chemical cue
combinations. Salamanders decreased the latency to first move in turbid conditions. Different letters indicate significant differences of p < 0.05.
to both predators and non-predators in the presence of visual cues,
suggesting the importance of chemical cues over visual cues for
accuracy in recognition (Mathis and Vincent, 2000; Hickman et al.,
2004). The reliance primarily on chemical cues may be owing to
their ubiquitous nature and persistence in freshwater (Ward and
Mehner, 2010) although visual cues are typically perceived quicker
than chemical signals (Endler, 1993). Alternatively, it may be owing
to decreased costs associated with chemical cues especially given
that E. sosorum is usually found under rocks and has reduced eyes. If
this is the case, then this species is using cues that match their perception strengths. Nonetheless, E. sosorum demonstrated the ability
to discriminate between the visual cues of a predator and the visual
cues of four non-predatory fish, which was then abated with the
addition of non-predator chemical cues.
When we explored latency to first move we found that salamander response to matched predator cues did not differ significantly
from matched or mismatched non-predator chemical cues, while
mismatched predator chemical cues differed significantly from
non-predator chemical cues. These results suggest that although
chemical cues are preferentially used for antipredator response,
visual cues may still contribute to their antipredator response.
The stronger response to mismatched predator chemical cues with
K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
non-predator visual cues may be attributed to the fact that this
treatment introduces a novel cue combination in a high threat environment (owing to the presence of predator chemical cues), which
may induce a heightened response due to threat aversion. Recent
studies have shown increased reaction to novel predator cues in
high risk environments (Brown et al., 2013, 2014; Chivers et al.,
2014; Brown et al., 2015), so it is possible that in such environments, signals that are not consistent with chemical cues elicit a
stronger response in terms of latency to first move. Alternatively,
the antipredator response is stronger because the salamanders perceived the four fish as a greater threat in the presence of predator
chemical cues (and they may not have been able to identify them
as predators vs non-predators).
Under turbid conditions, salamanders showed reduced
antipredator behavior to both predators and non-predators,
in the form of no change of activity and decreased latency to
first move, as compared to in clear conditions. This suggests that
either turbidity is interrupting chemical cues or that salamanders
perceive turbidity as a form of cover. The ‘turbidity as cover’/visual
refuge hypothesis predicts that predation risk decreases in turbid
conditions due to decreased conspicuousness of prey, making
reduction in antipredator behavior adaptive by reducing costs
associated with unnecessary antipredator behavior (Gregory,
1993; Ajemian et al., 2015). Our results indicate that while salamanders can use both visual and chemical cues for predator
recognition they may not compensate for information loss in
turbid environments. Although other studies have found that in
absence of complementary cues prey show a more risk-averse
response (Leduc et al., 2010; Elvidge and Brown, 2014), this is not
corroborated by our results showing reduced response in turbid
conditions.
Although turbidity can affect foraging of predators (Johansen
and Jones, 2013), we argue that it is unlikely that risk of predation
on E. sosorum is decreased in turbid conditions. In fact, predation
risk may be greater in turbid conditions in systems where only
predators are adapted to turbid conditions, where turbidity does
not affect the predator’s ability to forage, but decreases antipredator behavior in prey (Abrahams and Kattenfeld, 1997; Granqvist and
Mattila, 2004). Lepomis cyanellus is tolerant of turbidity extremes:
high turbidity does not affect the ability of L. cyanellus to forage or
attack (Heimstra et al., 1969). In addition, juveniles of the related
bluegill sunfish, L. macrochirus, had greatest foraging efficiency at
a low turbidity level (∼20 NTU) (Miner and Stein, 1993). Because E.
sosorum is more adapted to clear environments, turbidity may have
a greater impact on the ability of E. sosorum to detect predators
and less of an impact on the ability of L. cyanellus to capture prey,
thus making E. sosorum potentially more susceptible to predation.
Effects of turbidity on other behaviors, such as foraging and mating,
need to be assessed to determine the fitness impact of turbidity on
this endangered species.
The diminished antipredator behavior in turbid conditions has
conservation implications for E. sosorum. We studied a low turbidity value of 20 NTU, so our results are a conservative measure of
changes in antipredator behavior because turbidity levels spike to
double what we studied (White et al., 2003). Chemical cues may
be affected by the same particles that increase turbidity (Ferrari
et al., 2010b), which was not tested by our use of bentonite, so
future studies should examine how salamanders respond to environmental changes that affect more than one sensory modality.
Antipredator response to predators may be mediated by experience and turbidity could impact learning. van de Meutter et al.
(2005) found that antipredator behavior is decreased if organisms are reared and subsequently tested in turbid conditions but
antipredator behavior is unaffected when reared in clear conditions
and tested for response in turbid conditions. Further, Munoz and
Blumstein (2012) stress the importance of studying the interplay
9
between learning and turbidity for reintroduction purposes, indicating that determining the response of wild-caught salamanders,
which are both predator-experienced and turbid-experienced, is
of great importance. Therefore, experience with learning in turbid
conditions may be important, which can have significant implications for hatchery-raised species, especially those that are being
raised with the potential of reintroduction.
Acknowledgements
Many thanks to D. Cuevas for assistance with trials. Thanks to
J. Ott, C. Blake, K. Epp, A. Aspbury, and the EEB discussion group
for helpful advice and comments. Thanks to V. Cantu, K. Ostrand, J.
Crow, and the San Marcos Aquatic Resource Center for use of facilities, permits, and logistical help. This experiment was approved by
Texas State University IACUC (#0627 0802 15).
References
Abrahams, M., Kattenfeld, M., 1997. The role of turbidity as a constraint on
predator-prey interactions in aquatic environments. Behav. Ecol. Sociobiol. 40,
169–174.
Ajemian, M.J., Sohel, S., Mattila, J., 2015. Effects of turbidity and habitat complexity
on antipredator behavior of three-spined sticklebacks (Gasterosteus aculeatus).
Environ. Biol. Fishes 98, 45–55.
Brown, G.E., Cowan, J., 2000. Foraging trade-offs and predator inspection in an
ostariophysan fish: switching from chemical to visual cues. Behaviour 137,
181–195.
Brown, G.E., Ferrari, M.C.O., Elvidge, C.K., Ramnarine, I., Chivers, D.P., 2013.
Phenotypically plastic neophobia: a response to variable predation risk. Proc.
R. Soc. B 280, 20122712.
Brown, G.E., Chivers, D.P., Elvidge, C.K., Jackson, C.D., Ferrari, M.C.O., 2014.
Background level of risk determines the intensity of predator neophobia in
juvenile convict cichlids. Behav. Ecol. Sociobiol. 89, 127–133.
Brown, G.E., Demers, E.E., Joyce, B.J., Ferrari, M.C.O., Chivers, D.P., 2015. Retention
of neophobic predator recognition in juvenile convict cichlids; effects of
background risk and recent experience. Anim. Cogn. 18, 1331–1338.
Chivers, D.P., Al-Batati, F., Brown, G.E., Ferrari, M.C.O., 2013. The effect of turbidity
on recogntion and generalization of predators and non-predators in aquatic
ecosystems. Ecol. Evol. 3, 268–277.
Chivers, D.P., McCormick, M.I., Mitchell, M.D., Ramasamy, R.A., Ferrari, M.C.O.,
2014. Background level of risk determines how prey categorize predators and
non-predators. Proc. R. Soc. B 281, 20140355.
Collin, S.P., Whitehead, D., 2004. The functional roles of passive electroreception in
non-electric fishes. Anim. Biol. 54, 1–25.
Davies-Colley, R.J., Smith, D.G., 2001. Turbidity, suspended sediment, and water
clarity: a review. J. Am. Water Resour. Assoc. 37, 1085–1101.
Davis, D.R., Epp, K.J., Gabor, C.R., 2012. Predator generalization decreases the effect
of introduced predators in the San Marcos salamander, Eurycea nana. Ethology
118, 1191–1197.
Desantis, D.L., Davis, D.R., Gabor, C.R., 2013. Chemically mediated predator
avoidance in the Barton Springs Salamander (Eurycea sosorum). Herpetologica
69, 291–297.
Dries, L.A., Herrington, P.E., Colucci, L.A., Bendik, N.F., Chamberlain, B.S., David
Johns, P.G., Ed Peacock, P.E., 2013. Major Amendment and Extension of the
Habitat Conservation Plan for the Barton Springs Salamander (Eurycea
sosorum) and the Austin Blind Salamander (Eurycea waterlooensis) to Allow for
the Operation and Maintenance of Barton Springs and Adjacent Springs. City of
Austin, pp. 1–275.
Endler, J.A., 1993. Some general comments on the evolution and design of animal
communication systems. Philos. Trans. R. Soc. B 340, 215–225.
Elvidge, C.K., Brown, G.E., 2014. Predation costs of impaired chemosensory risk
assessment on acid-impacted juvenile Atlantic salmon (Salmo salar). Can. J.
Fish. Aquat. Sci. 71, 756–762.
Epp, K., Gabor, C.R., 2008. Innate and learned predator recognition mediated by
chemical signals in Eurycea nana. Ethology 114, 607–615.
Feng, L., Hu, C., Chen, X., Tian, L., Chen, L., 2012. Human induced turbidity changes
in poyang lake between 2000 and 2010: observations from MODIS. J. Geophys.
Res. Oceans 117 [C07006] http://dx.doi.org/10.1029/2011JC007864.
Ferrari, M.C.O., Chivers, D.P., 2009. Temporal variability threat sensitivity, and
conflicting information about the nature of risk: understanding the dynamics
of tadpole antipredator behavior. Anim. Behav. 78, 11–16.
Ferrari, M.C.O., Lysak, K.R., Chivers, D.P., 2010a. Turbidity as an ecological
constraint on learned predator recognition and generalization in a prey fish.
Anim. Behav. 79, 515–519.
Ferrari, M.C.O., Wisenden, B.D., Chivers, D.P., 2010b. Chemical ecology of
predator-prey interactions in aquatic ecosystems: a review and prospectus.
Can. J. Zool. 88, 698–724.
10
K.C. Zabierek, C.R. Gabor / Behavioural Processes 130 (2016) 4–10
Gadomski, D.M., Parsley, M.J., 2005. Effects of turbidity light level, and cover on
predation of white sturgeon larvae by prickly sculpins. Trans. Am. Fish. Soc.
134, 369–374.
Gillette, J.R., Peterson, M.G., 2001. The benefits of transparency: candling as a
simple method for determining sex in red-backed salamanders (Plethodon
cinereus). Herpetol. Rev. 32, 233–235.
Granqvist, M., Mattila, J., 2004. The effects of turbidity and light intensity on the
consumption of mysids by juvenile perch (Perca fluviatilis L.). Hydrobiologia
514, 93–101.
Gregory, R.S., 1993. Effect of turbidity on the predator avoidance behaviour of
juvenile chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci.
50, 241–246.
Hartman, E.J., Abrahams, M.V., 2000. Sensory compensation and the detection of
predators: the interaction between chemical and visual information. Philos.
Trans. R. Soc. B 267, 571–575.
Heimstra, N.W., Damkot, D.K., Benson, N.G., 1969. Some effects of silt turbidity on
behavior of juvenile largemouth bass and green sunfish. U.S. Bur. Sport Fish.
Wildl. Tech. Paper 20, 3–9.
Hemmi, J.M., 2005. Predator avoidance in fiddler crabs: 2. The visual cues. Anim.
Behav. 69, 615–625.
Henley, W.F., Patterson, M.A., Neves, R.J., Lemly, A.D., 2000. Effects of
sedimentation and turbidity on lotic food webs: a concise review for natural
resource managers. Rev. Fish. Sci. 8, 125–139.
Hettyey, A., Rolli, F., Thurlimann, N., Zurcher, A., Van Buskirk, J., 2012. Visual cues
contribute to predator detection in anuran larvae. Biol. J. Linnean Soc. 106,
820–827.
Hickman, C.R., Stone, M.D., Mathis, A., 2004. Priority use of chemical over visual
cues for detection of predators by graybelly salamanders, Eurycea multiplicata
griseogaster. Herpetologica 60, 203–210.
Horppila, J., Liljendahl-Nurminen, A., Malinen, T., 2004. Effects of clay turbidity and
light on the predator-prey interaction between smelts and chaoborids. Can. J.
Fish. Aquat. Sci. 61, 1862–1870.
IUCN, 2013. IUCN Red List of Threatened Species, Version 2013.2. http://www.
iucnredlist.org. Downloaded 10 March 2014.
Johansen, J.L., Jones, G.P., 2013. Sediment-induced turbidity impairs foraging
performance and prey choice of planktivorous coral reef fishes. Ecol App. 22,
1504–1517.
Johnstone, R.A., 1996. Multiple displays in animal communication: ‘backup signals’
and ‘multiple messages’. Philos. Trans. R. Soc. B 351, 329–338.
Kats, L.B., Dill, L.M., 1998. The scent of death: chemosensory assessment of
predation risk by prey animals. Ecoscience 5, 361–394.
Kiesecker, J.M., Chivers, D.P., Blaustein, A.R., 1996. The use of chemical cues in
predator recognition by western toad tadpoles. Anim. Behav. 52, 1237–1245.
Labay, B., Cohen, A.E., Sissel, B., Hendrickson, D.A., Martin, F.D., Sarkar, S., 2011.
Assessing historical fish community composition using surveys, historical
collection data, and species distribution models. PLoS One 6, e25145, http://dx.
doi.org/10.1371/journal.pone.0025145.
Leahy, S.M., McCormick, M.I., Mitchell, M.D., Ferrari, M.C., 2011. To fear or to feed:
the effects of turbidity on perception of risk by a marine fish. Biol. Lett. 7,
811–813.
Leduc, A.O.H.C., Kim, J., Macnaughton, C.J., Brown, G.E., 2010. Sensory complement
model helps to predict diel alarm response patterns in juvenile Atlantic salmon
(Salmo salar) under natural conditions. Can. J. Zool. 88, 398–403.
Lima, S.L., Steury, T., 2005. Perception of predation risk: the foundation of nonlethal
predator-prey interactions. In: Barbosa, P., Castellanos, I. (Eds.), Ecology of
Predator-prey Interactions. Oxford University Press, Oxford, p. 166–188.
Martín, J., Luque-Larena, J., López, P., 2009. When to run from an ambush predator:
balancing crypsis benefits with cost of fleeing in lizards. Anim. Behav. 78,
1011–1018.
Mathis, A., Vincent, F., 2000. Differential use of visual and chemical cues in
predator recognition and threat-sensitive predator evoidance responses by
larval newts (Notophthalmus viridescens). Can. J. Zool. 78, 1646–1652.
Mathis, A., Murray, K.L., Hickman, C.R., 2003. Do experience and body size play a
role in responses of larval ringed salamanders, Ambystoma annulatum, to
predator kairomones? Laboratory and field assays. Ethology 109, 159–170.
Miner, J.G., Stein, R.A., 1993. Interactive influence of turbidity and light on larval
bluegill (Lepomis macrochirus) foraging. Can. J. Fish. Aquat. Sci. 50, 781–788.
Munoz, N.E., Blumstein, D.T., 2012. Multisensory perception in uncertain
environments. Behav. Ecol. 23, 457–462.
Park, D., Lee, J., Ra, N., Eom, J., 2008. Male salamanders Hynobius leechi respond to
water vibrations via the mechanosensory lateral line system. J. Herpetol. 42,
615–625.
Ranåker, L., Anders Nilsson, P., Brönmark, C., 2012. Effects of degraded optical
conditions on behavioral responses to alarm cues in a freshwater fish. PLoS
One 7, e38411, http://dx.doi.org/10.1371/journal.pone.0038411.
Schmutzer, A.C., Gray, M.J., Burton, E.C., Miller, D.L., 2008. Impacts of cattle on
amphibian larvae and the aquatic environment. Freshw. Biol. 53, 2613–2625.
Secondi, J., Aumjaud, A., Pays, O., Boyer, S., Montembault, D., 2007. Water turbidity
affects the development of sexual morphology in the palmate newt. Ethology
119, 711–720.
Skelly, D.K., 1994. Activity level and the susceptibility of anuran larvae to
predation. Anim. Behav. 47, 465–468.
Stauffer, H.P., Semlitsch, R.D., 1993. Effects of visual: chemical and tactile cues of
fish on the behavioral responses of tadpoles. Anim. Behav. 46, 355–364.
Swanbrow Becker, L.J., Gabor, C.R., 2012. Effects of turbidity andv vs. chemical cues
on antipredator response in the endangered fountain darter (Etheostoma
fonticola). Ethology 118, 994–1000.
Thaker, M., Gabor, C.R., Fries, J.N., 2006. Sensory cues for conspecific associations in
aquatic San Marcos salamanders. Herpetologica 62, 151–155.
Tupa, D., Davis, W., 1976. Population dynamics of the San Marcos salamander
Eurycea nana. Tex. J. Sci. 27, 179–195.
Utne-Palm, A.C., 2002. Visual feeding of fish in a turbid environment: physical and
behavioral aspects. Mar. Freshw. Behav. Physiol. 35, 111–128.
van de Meutter, F., Stoks, R., De Meester, L., 2005. The effect of turbidity state and
microhabitat on macroinvertebrate assemblages: a pilot study of six shallow
lakes. Hydrobiologia 542, 379–390.
Walmsley, R.D., Butty, M., van der Piepen, H., Grobler, D., 1980. Light penetration
and the interrelationships between optical parameters in a turbid subtropical
impoundment. Hydrobiologia 70, 145–157.
Ward, A.J.W., Mehner, T., 2010. Multimodal mixed messages: the use of multiple
cues allows greater accuracy in social recognition and predator detection
decisions in the mosquitofish Gambusia holbrooki. Behav. Ecol. 21, 1315–1320.
Weissburg, M., Smee, D.L., Ferner, M.C., 2014. The sensory ecology of
nonconsumptive predator effects. Am. Nat. 184, 141–157.
White, J.A., Dwyer, F.J., Materna, E., Hardesty, D.K., Whites, D.W., 2003. Water
sediment quality in habitat springs of Edwards Aquifer salamanders. USFWS,
1–12.